In-Situ Metatranscriptomic Analyses Reveal the Metabolic Flexibility of the Thermophilic Anoxygenic Photosynthetic Bacterium <i>Chloroflexus</i><i>aggregans</i> in a Hot Spring Cyanobacteria-Dominated Microbial Mat

• Main Authors: Shigeru Kawai, Joval N. Martinez, Mads Lichtenberg, Erik Trampe, Michael Kühl, Marcus Tank, Shin Haruta, Arisa Nishihara, Satoshi Hanada, Vera Thiel
• Format: Article
• Language: English
• Published: MDPI AG 2021-03-01
• Series: Microorganisms
• Subjects: filamentous anoxygenic phototroph; microbial mats; hot springs; metatranscriptomics; energy metabolism; carbon fixation
• Online Access: https://www.mdpi.com/2076-2607/9/3/652

<i>Chloroflexus aggregans</i> is a metabolically versatile, thermophilic, anoxygenic phototrophic member of the phylum <i>Chloroflexota</i> (formerly <i>Chloroflexi</i>), which can grow photoheterotrophically, photoautotrophically, chemoheterotrophically, and chemoautotrophically. In hot spring-associated microbial mats, <i>C. aggregans</i> co-exists with oxygenic cyanobacteria under dynamic micro-environmental conditions. To elucidate the predominant growth modes of <i>C. aggregans</i>, relative transcription levels of energy metabolism- and CO₂ fixation-related genes were studied in Nakabusa Hot Springs microbial mats over a diel cycle and correlated with microscale in situ measurements of O₂ and light. Metatranscriptomic analyses indicated two periods with different modes of energy metabolism of <i>C. aggregans</i>: (1) phototrophy around midday and (2) chemotrophy in the early morning hours. During midday, <i>C. aggregans</i> mainly employed photoheterotrophy when the microbial mats were hyperoxic (400–800 µmol L⁻¹ O₂). In the early morning hours, relative transcription peaks of genes encoding uptake hydrogenase, key enzymes for carbon fixation, respiratory complexes as well as enzymes for TCA cycle and acetate uptake suggest an aerobic chemomixotrophic lifestyle. This is the first in situ study of the versatile energy metabolism of <i>C. aggregans</i> based on gene transcription patterns. The results provide novel insights into the metabolic flexibility of these filamentous anoxygenic phototrophs that thrive under dynamic environmental conditions.